Implications of aromatic-aromatic interactions: From protein structures to peptide models

Protein Science

Volumn 24, Issue 12, 2015, Pages 1920-1933

  Makwana, Kamlesh Madhusudan ^a   Mahalakshmi, Radhakrishnan ^a  

^a INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH BHOPAL   (India)

Author keywords

aromatic cluster; bionanomaterials; extremophiles; membrane proteins; peptide model; protein engineering; side chain interaction forces

Indexed keywords

AROMATIC AMINO ACID; AROMATIC COMPOUND; MEMBRANE PROTEIN; PEPTIDE; PROTEIN; PROTEIN BINDING;

ALPHA HELIX; AROMATIC AROMATIC INTERACTION; ARTICLE; BETA SHEET; CHEMICAL INTERACTION; CONFORMATIONAL TRANSITION; DNA PROTEIN COMPLEX; FLUORINATION; HIGH TEMPERATURE; HYDROGEN BOND; HYDROPHOBICITY; LIPID MEMBRANE; MOLECULAR RECOGNITION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; PSYCHROPHILIC BACTERIUM; STATIC ELECTRICITY; THERMOPHILIC BACTERIUM; THERMOSTABILITY; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PROTEIN TERTIARY STRUCTURE;

AMINO ACIDS, AROMATIC; MODELS, MOLECULAR; PEPTIDES; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEINS;

EID: 84957568168     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2814     Document Type: Article

References (115)

1. Chiti F, Dobson CM, (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333-366.
2. Gregersen N, Bross P, Vang S, Christensen JH, (2006) Protein misfolding and human disease. Annu Rev Genomics Hum Genet 7: 103-124.
3. Burley SK, Petsko GA, (1985) Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 229: 23-28.
4. Riley KE, Hobza P, (2013) On the importance and origin of aromatic interactions in chemistry and biodisciplines. Acc Chem Res 46: 927-936.
5. Baker CM, Grant GH, (2007) Role of aromatic amino acids in protein-nucleic acid recognition. Biopolymers 85: 456-470.
6. Asensio JL, Arda A, Canada FJ, Jimenez-Barbero J, (2013) Carbohydrate-aromatic interactions. Acc Chem Res 46: 946-954.
7. del Carmen Fernandez-Alonso M, Canada FJ, Jimenez-Barbero J, Cuevas G, (2005) Molecular recognition of saccharides by proteins. Insights on the origin of the carbohydrate-aromatic interactions. J Am Chem Soc 127: 7379-7386.
8. Kiehna SE, Laughrey ZR, Waters ML, (2007) Evaluation of a carbohydrate-pi interaction in a peptide model system. Chem Commun 4026-4028.
9. Dougherty DA, (1996) Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271: 163-168.
10. Ma JC, Dougherty DA, (1997) The cation-p interaction. Chem Rev 97: 1303-1324.
11. Dougherty DA, (2013) The cation-pi interaction. Acc Chem Res 46: 885-893.
12. Schottel BL, Chifotides HT, Dunbar KR, (2008) Anion-pi interactions. Chem Soc Rev 37: 68-83.
13. Valley CC, Cembran A, Perlmutter JD, Lewis AK, Labello NP, Gao J, Sachs JN, (2012) The methionine-aromatic motif plays a unique role in stabilizing protein structure. J Biol Chem 287: 34979-34991.
14. Reid K, Lindley P, Thornton J, (1985) Sulphur-aromatic interactions in proteins. FEBS Lett 190: 209-213.
15. Zauhar RJ, Colbert CL, Morgan RS, Welsh WJ, (2000) Evidence for a strong sulfur-aromatic interaction derived from crystallographic data. Biopolymers 53: 233-248.
16. Plevin MJ, Bryce DL, Boisbouvier J, (2010) Direct detection of CH/pi interactions in proteins. Nat Chem 2: 466-471.
17. Ganguly HK, Majumder B, Chattopadhyay S, Chakrabarti P, Basu G, (2012) Direct evidence for CH...pi interaction mediated stabilization of Pro-cisPro bond in peptides with Pro-Pro-aromatic motifs. J Am Chem Soc 134: 4661-4669.
18. Zondlo NJ, (2013) Aromatic-proline interactions: Electronically tunable CH/pi interactions. Acc Chem Res 46: 1039-1049.
19. Makwana KM, Mahalakshmi R, (2015) NMR analysis of tuning cross-strand Phe/Tyr/Trp-Trp interactions in designed beta-hairpin peptides: Terminal switch from L to D amino acid as a strategy for beta-hairpin capping. J Phys Chem B 119: 5376-5385.
20. Singh J, Thornton J, (1985) The interaction between phenylalanine rings in proteins. FEBS Lett 191: 1-6.
21. Hunter C, Singh J, Thornton J, (1991) Pi-pi interactions: the geometry and energetics of phenylalanine-phenylalanine interactions in proteins. J Mol Biol 218: 837-846.
22. Hunter C, Lawson K, Perkins J, Urch C, (2001) Aromatic interactions. J Chem Soc Perkin Trans 2: 651-669.
23. Sun S, Bernstein E, (1996) Aromatic van der Waals clusters: Structure and nonrigidity. J Phys Chem B 100: 13348-13366.
24. Goldstein RA, (2007) Amino-acid interactions in psychrophiles, mesophiles, thermophiles, and hyperthermophiles: insights from the quasi-chemical approximation. Protein Sci 16: 1887-1895.
25. Taylor TJ, Vaisman II, (2010) Discrimination of thermophilic and mesophilic proteins. BMC Struct Biol 10 (Suppl 1): S5
26. Meruelo AD, Han SK, Kim S, Bowie JU, (2012) Structural differences between thermophilic and mesophilic membrane proteins. Protein Sci 21: 1746-1753.
27. Siddiqui KS, Cavicchioli R, (2006) Cold-adapted enzymes. Annu Rev Biochem 75: 403-433.
28. Feller G, (2013) Psychrophilic enzymes: from folding to function and biotechnology. Scientifica 2013: 512840
29. Feller G, Arpigny J, Narinx E, Gerday C, (1997) Molecular adaptations of enzymes from psychrophilic organisms. Camp Biochem Physiol 118: 495-499.
30. Davail S, Feller G, Narinx E, Gerday C, (1994) Cold adaptation of proteins. Purification, characterization, and sequence of the heat-labile subtilisin from the antarctic psychrophile Bacillus TA41. J Biol Chem 269: 17448-17453.
31. Cipolla A, D'Amico S, Barumandzadeh R, Matagne A, Feller G, (2011) Stepwise adaptations to low temperature as revealed by multiple mutants of psychrophilic alpha-amylase from Antarctic bacterium. J Biol Chem 286: 38348-38355.
32. Anderson DE, Hurley JH, Nicholson H, Baase WA, Matthews BW, (1993) Hydrophobic core repacking and aromatic aromatic interaction in the thermostable mutant of T4 lysozyme Ser 117→Phe. Protein Sci 2: 1285-1290.
33. Mooers BH, Baase WA, Wray JW, Matthews BW, (2009) Contributions of all 20 amino acids at site 96 to the stability and structure of T4 lysozyme. Protein Sci 18: 871-880.
34. Kannan N, Vishveshwara S, (2000) Aromatic clusters: a determinant of thermal stability of thermophilic proteins. Protein Eng 13: 753-761.
35. Szilagyi A, Zavodszky P, (2000) Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure 8: 493-504.
36. Baldwin R, (1989) How does protein folding get started? Trends Biochem Sci 14: 291-294.
37. Dill KA, (1990) Dominant forces in protein folding. Biochemistry 29: 7133-7155.
38. Rees DC, DeAntonio L, Eisenberg D, (1989) Hydrophobic organization of membrane proteins. Science 245: 510-513.
39. Stevens TJ, Arkin IT, (1999) Are membrane proteins "inside-out" proteins? Proteins 36: 135-143.
40. Fiedler S, Broecker J, Keller S, (2010) Protein folding in membranes. Cell Mol Life Sci 67: 1779-1798.
41. Frank BS, Vardar D, Buckley DA, McKnight CJ, (2002) The role of aromatic residues in the hydrophobic core of the villin headpiece subdomain. Protein Sci 11: 680-687.
42. Schrödinger LLC, (2010) The PyMOL Molecular Graphics System, Version 12r3pre.
43. Budyak IL, Zhuravleva A, Gierasch LM, (2013) The role of aromatic-aromatic interactions in strand-strand stabilization of beta-sheets. J Mol Biol 425: 3522-3535.
44. Wimley WC, White SH, (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat Struct Biol 3: 842-848.
45. White SH, Wimley WC, (1999) Membrane protein folding and stability: physical principles. Annu Rev Biophys Biomol Struct 28: 319-365.
46. Killian JA, von Heijne G, (2000) How proteins adapt to a membrane-water interface. Trends Biochem Sci 25: 429-434.
47. Schlebach JP, Sanders CR, (2015) The safety dance: biophysics of membrane protein folding and misfolding in a cellular context. Q Rev Biophys 48: 1-34.
48. Cymer F, von Heijne G, White SH, (2015) Mechanisms of integral membrane protein insertion and folding. J Mol Biol 427: 999-1022.
49. Braun P, von Heijne G, (1999) The aromatic residues Trp and Phe have different effects on the positioning of a transmembrane helix in the microsomal membrane. Biochemistry 38: 9778-9782.
50. Chang YC, Bowie JU, (2014) Membrane protein folding stability and kinetics in bilayers. Protein Sci 23: 233-233.
51. Fleming KG, (2014) Energetics of membrane protein folding. Annu Rev Biophys 43: 233-255.
52. Hong H, (2014) Toward understanding driving forces in membrane protein folding. Arch Biochem Biophys 564: 297-313.
53. Otzen D, (2014) Membrane protein folding and stability. Arch Biochem Biophys 564: 262-264.
54. Kleinschmidt JH, Tamm LK, (1996) Kinetic studies on the refolding and membrane insertion of outer membrane protein a (Omp A) of E-coli. Biophys J 70: Mp139-Mp139.
55. Kleinschmidt JH, Tamm LK, (1996) Folding intermediates of a beta-barrel membrane protein. Kinetic evidence for a multi-step membrane insertion mechanism. Biochemistry 35: 12993-13000.
56. Kleinschmidt JH, den Blaauwen T, Driessen AJM, Tamm LK, (1999) Outer membrane protein A of Escherichia coli inserts and folds into lipid bilayers by a concerted mechanism. Biochemistry 38: 5006-5016.
57. Hong H, Park S, Jimenez RH, Rinehart D, Tamm LK, (2007) Role of aromatic side chains in the folding and thermodynamic stability of integral membrane proteins. J Am Chem Soc 129: 8320-8327.
58. Chaturvedi D, Mahalakshmi R, (2014) Juxtamembrane tryptophans have distinct roles in defining the OmpX barrel-micelle boundary and facilitating protein-micelle association. FEBS Lett 588: 4464-4471.
59. Gupta A, Zadafiya P, Mahalakshmi R, (2014) Differential contribution of tryptophans to the folding and stability of the attachment invasion locus transmembrane beta-barrel from Yersinia pestis. Sci Rep 4: 6508
60. Mahalakshmi R, (2015) Folding and stability of transmembrane beta-barrels of bacterial and human origin: Probing underlying similarities and principal differences using in vitro systems. Proc Indian Natn Sci Acad 81: 463-478.
61. Thomas A, Meurisse R, Charloteaux B, Brasseur R, (2002) Aromatic side-chain interactions in proteins. I. Main structural features. Proteins 48: 628-634.
62. Makwana KM, Mahalakshmi R, (2014) Asymmetric contribution of aromatic interactions stems from spatial positioning of the interacting aryl pairs in beta-hairpins. ChemBioChem 15: 2357-2360.
63. Samanta U, Pal D, Chakrabarti P, (1999) Packing of aromatic rings against tryptophan residues in proteins. Acta Cryst D55: 1421-1427.
64. Hill R, DeGrado W, (1998) Solution structure of α2D, a nativelike de novo designed protein. J Am Chem Soc 120: 1138-1145.
65. Bhattacharyya R, Samanta U, Chakrabarti P, (2002) Aromatic-aromatic interactions in and around alpha-helices. Protein Eng 15: 91-100.
66. Mahalakshmi R, Sengupta A, Raghothama S, Shamala N, Balaram P, (2005) Tryptophan-containing peptide helices: interactions involving the indole side chain. J Pept Res 66: 277-296.
67. Sengupta A, Mahalakshmi R, Shamala N, Balaram P, (2005) Aromatic interactions in tryptophan-containing peptides: crystal structures of model tryptophan peptides and phenylalanine analogs. J Pept Res 65: 113-129.
68. Santiveri CM, Jimenez MA, (2010) Tryptophan residues: scarce in proteins but strong stabilizers of beta-hairpin peptides. Biopolymers 94: 779-790.
69. Mahalakshmi R, Sengupta A, Raghothama S, Shamala N, Balaram P, (2007) Tryptophan rich peptides: influence of indole rings on backbone conformation. Biopolymers 88: 36-54.
70. Zhao CX, Polavarapu PL, Das C, Balaram P, (2000) Vibrational circular dichroism of beta-hairpin peptides. J Am Chem Soc 122: 8228-8231.
71. Tatko CD, Waters ML, (2001) Cross strand aromatic interactions in beta-turn peptides. Abstr Pap Am Chem Soc 222: U122-U122.
72. Andrew CD, Bhattacharjee S, Kokkoni N, Hirst JD, Jones GR, Doig AJ, (2002) Stabilizing interactions between aromatic and basic side chains in alpha-helical peptides and proteins. Tyrosine effects on helix circular dichroism. J Am Chem Soc 124: 12706-12714.
73. Butterfield S, Patel P, Waters ML, (2002) Contribution of aromatic interactions to α-helix stability. J Am Chem Soc 124: 9751-9755.
74. Tatko CD, Waters ML, (2002) Selective aromatic interactions in beta-hairpin peptides. J Am Chem Soc 124: 9372-9373.
75. Waters ML, (2002) Aromatic interactions in model systems. Curr Opin Chem Biol 6: 736-741.
76. Aravinda S, Shamala N, Das C, Sriranjini A, Karle IL, Balaram P, (2003) Aromatic-aromatic interactions in crystal structures of helical peptide scaffolds containing projecting phenylalanine residues. J Am Chem Soc 125: 5308-5315.
77. Aravinda S, Harini VV, Shamala N, Das C, Balaram P, (2004) Structure and assembly of designed beta-hairpin peptides in crystals as models for beta-sheet aggregation. Biochemistry 43: 1832-1846.
78. Tatko CD, Waters ML, (2004) Effect of halogenation on edge-face aromatic interactions in a beta-hairpin peptide: enhanced affinity with iodo-substituents. Org Lett 6: 3969-3972.
79. Waters ML, (2004) Aromatic interactions in peptides: impact on structure and function. Biopolymers 76: 435-445.
80. Andersen NH, Olsen KA, Fesinmeyer RM, Tan X, Hudson FM, Eidenschink LA, Farazi SR, (2006) Minimization and optimization of designed beta-hairpin folds. J Am Chem Soc 128: 6101-6110.
81. Palermo NY, Csontos J, Owen MC, Murphy RF, Lovas S, (2007) Aromatic-backbone interactions in model alpha-helical peptides. J Comput Chem 28: 2510-2510.
82. Santiveri CM, Leon E, Rico M, Jimenez MA, (2008) Context-dependence of the contiribution of disulfide bonds to beta-hairpin stability. Chem Eur J 14: 488-499.
83. Eidenschink L, Kier BL, Huggins KNL, Andersen NH, (2009) Very short peptides with stable folds: Building on the interrelationship of Trp/Trp, Trp/cation, and Trp/backbone-amide interaction geometries. Proteins 75: 308-322.
84. Mirassou Y, Santiveri CM, Perez de Vega MJ, Gonzalez-Muniz R, Jimenez MA, (2009) Disulfide bonds versus TrpTrp pairs in irregular beta-hairpins: NMR structure of vammin loop 3-derived peptides as a case study. ChemBioChem 10: 902-910.
85. Takekiyo T, Wu L, Yoshimura Y, Shimizu A, Keiderling TA, (2009) Relationship between hydrophobic interactions and secondary structure stability for Trpzip beta-hairpin peptides. Biochemistry 48: 1543-1552.
86. Wu L, McElheny D, Huang R, Keiderling TA, (2009) Role of tryptophan-tryptophan interactions in Trpzip beta-hairpin formation, structure, and stability. Biochemistry 48: 10362-10371.
87. Wu L, McElheny D, Takekiyo T, Keiderling TA, (2010) Geometry and efficacy of cross-strand Trp/Trp, Trp/Tyr, and Tyr/Tyr aromatic interaction in a beta-hairpin peptide. Biochemistry 49: 4705-4714.
88. Sonti R, Gopi HN, Muddegowda U, Ragothama S, Balaram P, (2013) A designed three-stranded beta-sheet in an alpha/beta hybrid peptide. Chem Eur J 19: 5955-5965.
89. Matsumoto M, Lee SJ, Gagne MR, Waters ML, (2014) Cross-strand histidine-aromatic interactions enhance acyl-transfer rates in beta-hairpin peptide catalysts. Org Biomol Chem 12: 8711-8718.
90. Popp A, Wu L, Keiderling TA, Hauser K, (2014) Effect of hydrophobic interactions on the folding mechanism of beta-hairpins. J Phys Chem B 118: 14234-14242.
91. Koradi R, Billeter M, Wuthrich K, (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14: 51-55. 29-32.
92. Cochran AG, Skelton NJ, Starovasnik MA, (2001) Tryptophan zippers: stable, monomeric beta -hairpins. Proc Natl Acad Sci USA 98: 5578-5583.
93. Makwana KM, Raghothama S, Mahalakshmi R, (2013) Stabilizing effect of electrostatic vs. aromatic interactions in diproline nucleated peptide beta-hairpins. Phys Chem Chem Phys 15: 15321-15324.
94. Makwana KM, Mahalakshmi R, (2014) Comparative analysis of cross strand aromatic-Phe interactions in designed peptide beta-hairpins. Org Biomol Chem 12: 2053-2061.
95. Makwana KM, Mahalakshmi R, (2015) Nature of aryl-tyrosine interactions contribute to beta-hairpin scaffold stability: NMR evidence for alternate ring geometry. Phys Chem Chem Phys 17: 4220-4230.
96. Viguera AR, Jimenez MA, Rico M, Serrano L, (1996) Conformational analysis of peptides corresponding to beta-hairpins and a beta-sheet that represent the entire sequence of the alpha-spectrin SH3 domain. J Mol Biol 255: 507-521.
97. Setnicka V, Huang R, Thomas CL, Etienne MA, Kubelka J, Hammer RP, Keiderling TA, (2005) IR study of cross-strand coupling in a beta-hairpin peptide using isotopic labels. J Am Chem Soc 127: 4992-4993.
98. Nesloney CL, Kelly JW, (1996) A 2,3'-substituted biphenyl-based amino acid facilitates the formation of a monomeric beta-hairpin-like structure in aqueous solution at elevated temperature. J Am Chem Soc 118: 5836-5845.
99. Jager M, Dendle M, Fuller AA, Kelly JW, (2007) A cross-strand Trp Trp pair stabilizes the hPin1 WW domain at the expense of function. Protein Sci 16: 2306-2313.
100. Pace CJ, Kim D, Gao J, (2012) Experimental evaluation of CH-pi interactions in a protein core. Chem Eur J 18: 5832-5836.
101. Pace CJ, Gao J, (2013) Exploring and exploiting polar-pi interactions with fluorinated aromatic amino acids. Acc Chem Res 46: 907-915.
102. Woll MG, Hadley EB, Mecozzi S, Gellman SH, (2006) Stabilizing and destabilizing effects of phenylalanine -> F5-phenylalanine mutations on the folding of a small protein. J Am Chem Soc 128: 15932-15933.
103. Lanzarotti E, Biekofsky RR, Estrin DA, Marti MA, Turjanski AG, (2011) Aromatic-aromatic interactions in proteins: beyond the dimer. J Chem Inf Model 51: 1623-1633.
104. Gray HB, Winkler JR, (2015) Hole hopping through tyrosine/tryptophan chains protects proteins from oxidative damage. Proc Natl Acad Sci USA 112:10920-10925
105. Reches M, Gazit E, (2003) Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 300: 625-627.
106. Marek P, Abedini A, Song B, Kanungo M, Johnson ME, Gupta R, Zaman W, Wong SS, Raleigh DP, (2007) Aromatic interactions are not required for amyloid fibril formation by islet amyloid polypeptide but do influence the rate of fibril formation and fibril morphology. Biochemistry 46: 3255-3261.
107. Tu LH, Raleigh DP, (2013) Role of aromatic interactions in amyloid formation by islet amyloid polypeptide. Biochemistry 52: 333-342.
108. Frederix PW, Scott GG, Abul-Haija YM, Kalafatovic D, Pappas CG, Javid N, Hunt NT, Ulijn RV, Tuttle T, (2015) Exploring the sequence space for (tri-)peptide self-assembly to design and discover new hydrogels. Nature Chem 7: 30-37.
109. Sievers SA, Karanicolas J, Chang HW, Zhao A, Jiang L, Zirafi O, Stevens JT, Munch J, Baker D, Eisenberg D, (2011) Structure-based design of non-natural amino-acid inhibitors of amyloid fibril formation. Nature 475: 96-100.
110. Bram Y, Lampel A, Shaltiel-Karyo R, Ezer A, Scherzer-Attali R, Segal D, Gazit E, (2015) Monitoring and targeting the initial dimerization stage of amyloid self-assembly. Angew Chem Int Ed Engl 54: 2062-2067.
111. Tu LH, Young LM, Wong AG, Ashcroft AE, Radford SE, Raleigh DP, (2015) Mutational analysis of the ability of resveratrol to inhibit amyloid formation by islet amyloid polypeptide: critical evaluation of the importance of aromatic-inhibitor and histidine-inhibitor interactions. Biochemistry 54: 666-676.
112. Pellach M, Atsmon-Raz Y, Simonovsky E, Gottlieb H, Jacoby G, Beck R, Adler-Abramovich L, Miller Y, Gazit E, (2015) Spontaneous structural transition in phospholipid-inspired aromatic phosphopeptide nanostructures. ACS Nano 9: 4085-4095.
113. Mahajan M, Bhattacharjya S, (2013) Beta-hairpin peptides: heme binding, catalysis, and structure in detergent micelles. Angew Chem Int Ed Engl 52: 6430-6434.
114. Mahajan M, Bhattacharjya S, (2014) Designed di-heme binding helical transmembrane protein. ChemBioChem 15: 1257-1262.
115. Fleming S, Ulijn RV, (2014) Design of nanostructures based on aromatic peptide amphiphiles. Chem Soc Rev 43: 8150-8177.